Abstract
In the coastal areas of Japan, three species of greenling (Hexagrammos spp.) can hybridize. In a natural reef setting we showed that Hexagrammos agrammus and H. octogrammus established their breeding territories in a shallow area where seaweed was abundant, whereas H. otakii established breeding territories in a deep area that was sparsely covered with seaweed. This difference in habitat use resulted in H. otakii being distributed separately from the other two species, thereby reducing the potential for hybridization. However, all the three species co-occurred in an artificial area near a breakwater. This area is characterized by steep slopes and complex stacked concrete structures, which create a mosaic-habitat consisting of a shallow environment with seaweed and a deep environment with sparse seaweed, allowing the three species to breed within a single area. Our results suggest that man-made structures can create an artificial mosaic-habitat that can disrupt habitat isolation and promote hybridization between species.
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References
Amaoka K (1984) Family Hexagrammidae. In: Masuda H, Amaoka K, Araga C, Urno T, Yoshino T (eds) The fishes of the Japanese Archipelago (in Japanese). Tokai University Press, Tokyo, pp 320–321
Arnold ML (1997) Natural hybridization and evolution. Oxford University Press, New York
Balanov AA, Markevich AI, Antonenko DV, Crow KD (2001) The first occurrence of hybrids of Hexagrammos otakii × H. octogrammus and description of H. otakii from Peter the Great Bay (The Sea of Japan). J Ichthyol 41:728–738
Bierne N, Bonhomme F, David P (2003) Habitat preference and the marine-speciation paradox. Proc R Soc Lond B Biol Sci 270:1399–1406
Bridle JR, Baird SJE, Butlin RK (2001) Spatial structure and habitat variation in a grasshopper hybrid zone. Evolution 55:1832–1843
Coyne JA, Orr HA (2004) Speciation. Sinauer Associates Inc, Massachusetts
Crow KD, Powers DA, Bernardi G (1997) Evidence for multiple maternal contributors in nests of kelp greenling (Hexagrammos decagrammus, Hexagrammidae). Copeia 1997:9–15
Crow KD, Munehara H, Kanamoto Z, Balanov A, Antonenko D, Bernardi G (2007) Maintenance of species boundaries despite rampant hybridization between three species of reef fishes (Hexagrammidae): implications for the role of selection. Biol J Linn Soc Lond 91:135–147
Eisenhour DJ, Piller KR (1997) Two new intergeneric hybrids involving Semotilus atromaculatus and the genus Phoxinus with analysis of additional Semotilus atromaculatus–Phoxinus hybrids. Copeia 1997:204–209
Estrada C, Jiggins CD (2002) Patterns of pollen feeding and habitat preference among Heliconius species. Ecol Entomol 27:448–456
Gorbunova NN (1970) Spawning and development of greenlings (Family Hexagrammidae). In: Rass TS (ed) Greenlings: taxonomy, biology and interoceanic transplantation. Israel Program for Scientific Translations, Moskva, pp 121–185
Kanamoto Z (1976a) On the ecology of Hexagrammid fish. 1) Habitats and behaviors of Agrammus agrammus (Temminck et Schlegel) and Hexagrammos otakii (Jordan et Starks) (in Japanese with English abstract). Jpn J Ecol 26:1–12
Kanamoto Z (1976b) On the ecology of Hexagrammid fish. 2) The distribution of Hexagrammid fish (in Japanese). Nihon suisan gakkai tohoku sibu kaiho 26:48–53
Lamb T, Avise JC (1986) Directional introgression of mitochondrial DNA in a hybrid population of tree frogs: the influence of mating behavior. Proc Natl Acad Sci USA 8:2526–2530
Levin DA, Francisco-Ortega J, Jansen RK (1996) Hybridization and the extinction of rare plant species. Conserv Biol 10:10–16
Mayr E (1963) Animal species and evolution. Belknap Press of Harvard University Press, Cambridge
Munehara H (2001) Mating and paternal care behavior of Hexagrammid fishes. In: Amaoka K (ed) The story of fishes––biodiversity of fishes (in Japanese). Tokai University Press, Tokyo, pp 151–167
Munehara H, Kanamoto Z, Miura T (2000) Spawning behavior and interspecific breeding in three Japanese greenlings (Hexagrammidae). Ichthyol Res 47:287–292
Nosil P, Vines TH, Funk DJ (2005) Perspective: reproductive isolation caused by natural selection against immigrants from divergent habitats. Evolution 59:705–719
Oshima Y, Nakamura C (1942) Life history of Hexagrammos otakii (in Japanese). Suisangaku kaihou 9:81–89
Rhymer JM, Simberloff D (1996) Extinction by hybridization and introgression. Annu Rev Ecol Syst 27:83–109
Ross CL, Harrison RG (2002) A fine-scale spatial analysis of the mosaic hybrid zone between Gryllus firmus and Gryllus pennsylvanicus. Evolution 56:2296–2312
Ross CL, Benedix JH, Garcia C, Lambeth K, Perry R, Selwyn V, Howard DJ (2008) Scale-independent criteria and scale-dependent agents determining the structure of a ground cricket mosaic hybrid zone (Allonemobius socius–Allonemobius fasciatus). Biol J Linn Soc Lond 94:777–796
Rutenberg EP (1970) Survey of the fishes of family Hexagrammidae. In: Rass TS (ed) Greenlings: taxonomy, biology and interoceanic transplantation. Israel Program for Scientific Translations, Moskva, pp 1–103
Schlefer EK, Romano MA, Guttman SI, Rush SB (1986) Effects of twenty years of hybridization in a disturbed habitat on Hyla cinerea and Hyla gratiosa. J Herpetol 20:210–221
Scribner KT, Page KS, Bartron ML (2001) Hybridization in freshwater fishes: a review of case studies and cytonuclear methods of biological inference. Rev Fish Biol Fish 10:293–323
Seehausen O, Takimoto G, Roy D, Jokela J (2008) Speciation reversal and biodiversity dynamics with hybridization in changing environments. Mol Ecol 17:30–44
Takahashi A, Tsaur SC, Coyne JA, Wu CI (2001) The nucleotide changes governing cuticular hydrocarbon variation and their evolution in Drosophila melanogaster. Proc Natl Acad Sci USA 98:3920–3925
Takayama T (2004) Breakwater. In: Japanese Association for Coastal Zone Studies (ed) Encyclopedia of coastal zone environment (in Japanese). Kyoritsu Shuppan, Tokyo, pp 83–84
Wolf DE, Takebayashi N, Rieseberg LH (2001) Predicting the risk of extinction through hybridization. Conserv Biol 15:1039–1053
Yamamoto G, Nishioka C (1948) Breeding habits and developmental process of greenling; Hexagrammos otakii Jordan & Starks (in Japanese with English abstract). Seibutu 3:167–170
Yanchukov A, Hofman S, Szymura JM, Mezhzherin SV (2006) Hybridization of Bombina bombina and B-variegata (Anura, Discoglossidae) at a sharp ecotone in western Ukraine: comparisons across transects and over time. Evolution 60:583–600
Acknowledgments
The authors thank Drs. Masakado Kawata, John Bower, Satoshi Awata, Yoko Iwata, Karen Crow, and Ayumi Tezuka for reading this manuscript and providing valuable comments, Drs. H. Yasui, H. Mizuta and T. Kawagoe for advice on the classification of seaweeds, and Dr. S. Mawatari for identification of bryozoans. This work was supported by a grant in aid for scientific research from the Ministry of Education.
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Kimura, M.R., Munehara, H. The disruption of habitat isolation among three Hexagrammos species by artificial habitat alterations that create mosaic-habitat. Ecol Res 25, 41–50 (2010). https://doi.org/10.1007/s11284-009-0624-3
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DOI: https://doi.org/10.1007/s11284-009-0624-3